Knowledge, Attitudes, and Practices of Private Sector Immunization Service Providers in Gujarat, India
SUBMITTED DRAFT UNDER PEER REVIEW
José E. Hagana, b, Narayan Gaonkarc, Vikas Doshid, Anas Patnie, Shailee Vyase, Vihang Mazumdard, J K Kosambiyae,
Satish Guptaf, Margaret Watkinsa
a) Global Immunization Division, Centers for Disease Control and Prevention, Atlanta, USA
b) Epidemic Intelligence Service, Centers for Disease Control and Prevention, Atlanta, USA
c) United Nations Children’s Fund, Gujarat, India
d) Department of Preventive and Social Medicine, Medical College Baroda, Baroda, India
e) Department of Preventive and Social Medicine, Government Medical College, Surat, India
f) United Nations Children’s Fund, Delhi, India
Corresponding author: Jose Hagan: [email protected]. Tel: +1 404 718 6361. Fax: +1 404 471 8414
Author emails:
Jose Hagan [email protected]
Narayan Gaonkar [email protected]
Vikas Doshi [email protected]
Anas Patni [email protected]
Shailee Vyas [email protected]
Vihang Mazumdar [email protected]
J K Kosambiya [email protected]
Satish Gupta [email protected]
Margaret Watkins [email protected]
mailto:[email protected]:[email protected]:[email protected]:[email protected]:[email protected]:[email protected]:[email protected]:[email protected]:[email protected]:[email protected]
Abstract
Background: India is responsible for 30% of the annual global cohort of unvaccinated children worldwide.
Private practitioners provide an estimated 21% of vaccinations in urban centers of India, and are important
partners in achieving high vaccination coverage.
Methods: We used an in-person questionnaire and on-site observation to assess knowledge, attitudes, and
practices of private immunization service providers regarding delivery of immunization services in the urban
settings of Surat and Baroda, in Gujarat, India. We constructed a comprehensive sampling frame of all private
physician providers of immunization services in Surat and Baroda cities, by consulting vaccine distributors, local
branches of physician associations, and published lists of private medical practitioners. All providers were
contacted and asked to participate in the study if they provided immunization services. Data were collected
using an in-person structured questionnaire and directly observing practices; one provider in each practice
setting was interviewed.
Results: The response rate was 82% (121/147) in Surat, and 91% (137/151) in Baroda. Of 258 participants 195
(76%) were pediatricians, and 63 (24%) were general practitioners. Practices that were potential missed
opportunities for vaccination (MOV) included not strictly following vaccination schedules if there were concerns
about ability to pay (45% of practitioners), and not administering more than two injections in the same visit
(60%). Only 22% of respondents used a vaccination register to record vaccine doses, and 31% reported vaccine
doses administered to the government. Of 237 randomly selected vaccine vials, 18% had expired vaccine vial
monitors.
Conclusions: Quality of immunization services in Gujarat can be strengthened by providing training and support
to private immunization service providers to reduce MOVs and improve quality and safety; other more context
specific strategies that should be evaluated may involve giving feedback to providers on quality of services
delivered and working through professional societies to adopt standards of practice.
Keywords: Health Knowledge, Attitudes, Practice; Public-Private Sector Partnerships; Private Sector;
Vaccination;
Background
India leads the world in number of childhood deaths [1], is responsible for 30% of the annual global cohort of
unvaccinated children [2], and accounts for 47% of global measles mortality [3]. In 2015, through routine
immunization programs, only 82% of India’s children received three doses of oral polio vaccine (OPV3) [4];
during 2014, estimated state-level percentage of children aged 9—11 months who had been fully vaccinated
(i.e., having received bacille Calmette–Guérin [BCG], three doses of diphtheria-pertussis-tetanus vaccine [DPT3],
three doses of OPV3, and one dose of measles-containing virus [MCV1]), ranged from 27% to 89% [5]. While
strategies for measles elimination and polio eradication have focused on improving vaccination coverage and
access to services in the public sector, the private health care sector, comprising a wide range of for-profit and
not-for-profit practices, also plays a large and important role in India. In 2013, expenditures in the private sector
accounted for 68% of total health expenditures country-wide [6], and an estimated 21% of routine childhood
vaccinations in urban areas of India are provided in the private sector [7].
The few studies that have explored the role of the private sector in immunization service delivery in low- and
middle-income countries have generally found less knowledge of recommended immunization services and
lower quality of service delivery among private sector providers when compared to their public sector
counterparts [8]. Globally the pooled prevalence of missed opportunities for vaccination (MOV) for children, in
which a person eligible for vaccination, and with no valid contraindication, visits a health service facility and
does not receive all of the recommended vaccines, is estimated at 32% among low- and middle-income
countries [9]. Little is known, however, about the specific behaviors and practices among private sector
providers that could be targeted to decrease this high prevalence. In studies conducted in India, private sector
providers had less concern about polio, greater likelihood to depart from recommended vaccine schedules, and
lower sense of personal responsibility for providing vaccinations, than did providers in the public sector [10–12].
However, these studies were limited to members of the Indian Academy of Pediatrics (IAP) in Bihar and Uttar
Pradesh, and were limited to attitudes rather than actual practices.
Because of limitations of previous studies and the lack of on-site observational assessment of immunization
practices, many questions remain about actual immunization practices in the private sector setting in India, and
the role that practice changes can play in improving vaccination coverage. To address this knowledge gap, we
conducted a study among private providers who offered child vaccination in two urban settings in Gujarat State,
India. Gujarat is a state in Western India, which, like many population centers in India, is urbanizing rapidly
(currently 43% urban) and has experienced rapid economic growth that is outpacing growth of social and
development metrics. In urban Gujarat state, private immunization providers deliver a large percentage (24%) of
immunization services, similar to other urban areas of India [7]. The second and third most populous cities in
Gujarat State were selected for this study, Surat (pop. 4,591,246), and Baroda (pop. 1,822,221).
The objectives of our study were to assess: a) the knowledge, attitudes, and practices of private providers
regarding administration of polio, measles and other vaccines, including vaccination schedules, cold chain
storage of vaccines, recording vaccine doses administered, and vaccine management; b) acute flaccid paralysis
(AFP) and measles case reporting; and c) the feasibility of potential public-private partnership strategies to
improve access to immunizations in urban populations.
Methods
Survey design
We conducted a systematic assessment of urban private medical providers who offer childhood immunizations
in Surat and Baroda municipal corporations in Gujarat State, India. A comprehensive sampling frame of private
immunization providers was created by obtaining a list of vaccine purchasers from the major vaccine distributors
in these two cities, accounting for approximately 90% of the combined market. This list was supplemented with
membership lists of the Surat and Baroda Branches of both the Indian Academy of Pediatrics and the General
Practitioner Association, and other published directories of pediatricians (defined as practitioners with an MBBS
degree, plus a diploma in pediatrics, or MD in pediatrics) and general practitioners (MBBS degrees without
further specialization) from the region. Finally, snowball sampling was used to identify additional providers that
were not captured through the previous methods [13].
All identified practitioners were contacted by telephone to determine whether they provide immunization
services to children in a practice located within the city limits. All practitioners were offered the opportunity to
participate in the study if they provided immunization services in any non-governmental setting, including both
for-profit and not-for-profit practices, such as charity or faith-based organizations. In the case of provider groups
that share common immunization practices and supplies, a provider who was familiar with the common
practices among the group was selected for interview. Practitioners were not required to offer a specific
minimum set of vaccines to be eligible to participate; however, practitioners were excluded from the study if
they did not provide vaccines to children as part of the routine childhood immunization schedule.
Representatives of IAP, Indian Medical Association, and the Gujarat Department of Health and Family Welfare
were consulted during study design and pilot testing of the questionnaire, which was performed among
pediatricians in Ahmedabad city to avoid exposing potential study participants in Surat and Baroda to the
questionnaire.
Measures
Each assessment included administration of an in-person structured questionnaire, which captured information
on knowledge, attitudes and practices related to vaccination schedules, potential MOV, record-keeping of
vaccine doses administered, injection safety, vaccine management and storage, and reporting of vaccination
coverage, adverse events following immunization (AEFI), and notifiable diseases. In addition, we directly
observed practices for vaccine management and storage, and safety of vaccine administration. Vaccine
refrigerators were examined for the presence of thermometers and temperature logs and non-vaccines,
including food, and other medications. One vaccine vial was randomly selected from each refrigerator and the
vaccine vial monitor (VVMs) was examined.
We also assessed practitioner’s willingness to enter into partnerships with the government to deliver subsidized
vaccine and improve vaccine dose administration reporting. Practitioners were asked to rate the acceptability of
three example partnership models: “Allow the government to use my facility to administer free vaccines to the
public”, “Receive some free vaccines from the government in exchange for me reporting the number of doses
given, and I could not charge any fee”, and “Receive some free vaccines from the government in exchange for
me reporting the number of doses given, and I could charge a fee”.
Data collection and analysis
The assessments were conducted by trained interviewers composed of faculty members and residents from the
Department of Preventive and Social Medicine at Surat and Baroda Medical colleges. Data were collected on
paper case report forms, double entered and managed using REDCap electronic data capture tools [14]. R
statistical programming language v.3.2.3 [15] was used for descriptive analyses using chi-square or Fisher’s exact
tests, as appropriate. P-value cut-offs for statistical significance were determined after adjusting for false
discovery rate due to multiple comparisons [16].
Results
Overall provider response rate was 87% (258/298), 82% (121/147) in Surat, and 91% (137/151) in Baroda.
Characteristics of physicians and their practices are described in Table 1. Pediatricians comprised the majority of
providers (195, 76%), and the remaining 63 (24%) were general practitioners. A wide range of vaccines were
offered by private sector providers (Table 2), including vaccines not available in India’s Universal Immunization
Program (UIP) schedule. In general, private providers closely followed the IAP-recommended vaccination
schedule, rather than the UIP schedule (the IAP schedule includes inactivated polio, pneumococcal conjugate,
rotavirus, varicella, hepatitis A, typhoid, human papillomavirus, and measles-mumps-rubella vaccines ).
We assessed vaccination practices of practitioners to identify potential MOV (Table 3). Most practitioners (60%)
were unwilling to administer three vaccines in the same visit. Of those, 77% reported they did not administer
three concurrent injections because of their own judgement, rather than parental concerns (21%) or other
motivations. In addition, 45% of practitioners stated that they would vary the vaccination schedule “sometimes
or often” for financial reasons, e.g., concerns about caregiver’s ability to pay for multiple vaccines at the same
time.
Recordkeeping and reporting practices were suboptimal (Table 3). Twenty-two percent of practitioners reported
using a register to record vaccination doses. In addition, 51% responded they would not vaccinate if the parents
did not bring the child’s vaccination card. A majority (69%) of practitioners stated they do not report vaccine
doses administered to the government. Practitioners commonly responded that they would not report cases
that met surveillance definitions for notifiable diseases including measles (88%) and polio (36%). The most
common reason given for not reporting was not being aware of any reporting requirement.
We directly observed several practices suggesting weakness in vaccine safety and cold-chain quality (Table 3). In
almost all practices (92%), vaccines were stored in domestic refrigerators. Expired (stage 3—4) VVMs were
noted in 18% of observed refrigerators. We observed notable outlier practices with respect to stock
management; some providers did not maintain refrigerators for vaccine storage, and kept vaccine vials in
unrefrigerated thermal boxes (7%), or obtained vaccine vials directly from a nearby pharmacy as needed on a
patient-by-patient basis (
the India Academy of Pediatrics. The response rate for this study (87%) was also higher than in prior studies
(range 47-51% among pediatricians) [10–12]. We aimed to maximize the completeness of the sample of
providers who vaccinate by obtaining the actual lists of vaccine purchasers from vaccine distributors in the two
cities. We were therefore able to capture information from multiple categories of physician immunization
providers in Gujarat irrespective of membership in professional organizations.
Our study among private providers in Gujarat found a high prevalence of practices that lead to MOV, such as
multiple injection hesitancy. Several studies have demonstrated that concern about multiple injections among
providers is associated with vaccination delay and incomplete vaccinations [18–21]. Although providers in our
study reported some reluctance from parents towards multiple vaccinations, providers often overestimate this
parental concern [22]. In addition, since most providers in our study reported their own reluctance to administer
multiple vaccinations at the same visit, multiple injection hesitancy among practitioners might be a key source of
MOV that can be addressed in India.
Our findings suggest that MOV in the private sector could be reduced by relatively straight-forward changes in
practice, such as performing opportunistic screening for vaccination status and appropriate vaccination by
providers at all visits. MOV could also be reduced through the improved and increased use of office-based
records and child-based vaccination registers, instead of relying solely on home-based vaccination cards; half of
the providers responded that they would not vaccinate a child who presented for immunizations without their
home-based vaccination card. In addition, other more context-specific strategies to improve provider practices
might be needed, including working through professional societies to adopt standards of practice on multiple
vaccinations and recordkeeping, for example, and giving feedback to providers through on quality of services
delivered. Although only rigorously evaluated in high income countries, provider assessment and feedback
interventions are powerful evidence-based strategies to improve vaccination coverage; these strategies both
evaluate provider performance in delivering one or more vaccinations to a client population (assessment) and
present providers with information about their performance (feedback) [23]. In addition, MOV cannot be fully
addressed without a key change in the attitude of practitioners towards immunization; without a specific valid
contraindication, every child should be vaccinated with all indicated vaccines to reach and maintain high
vaccination coverage [24,25].
We found a wide range of quality in cold chain and injection safety practices. Any blood borne pathogen
transmission event that occurs in the private sector due to unsafe injection practices, or vaccine preventable
disease outbreak among vaccinated children due to improper cold-chain storage practices, would be highly
visible and threaten to undermine public trust in the UIP; therefore, training on injection safety, and cold-chain
maintenance, including the appropriate use and interpretation of VVMs and temperature monitoring practices
may be valuable. We did not obtain information on the cold-chain, transportation, and quality assurance
systems used by vaccine distributors; future assessments focused on vaccine distributor supply and quality
would also be informative.
Finally, we found a great need to clarify and communicate about existing channels for private sector providers to
report vaccination doses to reliably estimate vaccination coverage; AEFI to identify and monitor vaccine safety;
and notifiable vaccine-preventable diseases, to monitor the impact of vaccination. In particular, with the recent
switch to bivalent oral poliovirus vaccine (bOPV) and inactivated poliovirus vaccine (IPV) introduction, ongoing
sensitive AFP surveillance is needed to identify potential circulating poliovirus in India.
Although acceptability of the public-private partnership models that we investigated showed variation by city
and level of training of the provider, none of the three models in either city were accepted by more than about
half of providers surveyed, and no model had greater than 44% acceptability overall. Exploring the acceptability
of the public-private partnership models further will likely require the use of qualitative methods (e.g., focus
groups or key informant interviews) at several levels in the health system to understand barriers and identify
meaningful public–private partnership models.
This study has some limitations. Our study was designed to provide a description of attitudes and practices
related to immunization services among all physicians offering these services in two major cities in Gujarat state.
However, these findings might not be representative of all urban settings in India, which range widely in level of
economic development and other factors such as religious and cultural norms that influence demand, access,
and use of the health care system, as well as norms, attitudes, and practices among health care providers. In
addition, although our study aimed to obtain a comprehensive sample of private immunization service
providers, no central registration of medical practitioners is available that could be used to generate a complete
sampling frame, and physician associations do not exist at a national or state level for general practice
physicians or non-physician providers. Although non-physicians provide immunization services in some settings
in India, we were unsuccessful in obtaining municipal membership lists of non-physician immunization providers
affiliated with Ayurvedic Yoga and Naturopathy, Unani, Siddha, and Homeopathy organizations; we limited our
assessment to private practitioners. A similar study of immunization practices in India’s UIP would be valuable to
allow comparison of the two groups. Finally, our findings should be interpreted cautiously, given the potential
for social desirability bias in the responses, or the desire of providers not to provide information that might be
used to increase regulation or estimate income for the purposes of taxation.
This study provides key information that should influence development of mutually strengthening relationships
between the public and private health sector, and policies related to private vaccination provider practices in
Gujarat. Immunization services can be strengthened in this State by engaging the private sector to leverage the
important position it plays in ensuring high vaccine coverage in the State, while reducing MOV, strengthening
cold-chain and injection safety practices, improving recordkeeping and reporting practices, and exploring
innovative and mutually-beneficial partnerships.
Conflicts of Interest Statement: The authors declare no conflicts of interest.
Acknowledgements: This research did not receive any specific grant from funding agencies in the public,
commercial, or not-for-profit sectors.
Figure captions:
Figure 1. Acceptability of example public-private partnership models among vaccination providers, stratified by
city (left panel) and by level of training (right panel). Percentages within the figure refer to respondents in
overall disagreement (disagree or strongly disagree, left), neutral or undecided (center), and in overall
agreement (agree or strongly agree, right).
References
[1] Black RE, Cousens S, Johnson HL, Lawn JE, Rudan I, Bassani DG, et al. Global, regional, and national causes
of child mortality in 2008: a systematic analysis. Lancet 2010;375:1969–87. doi:10.1016/S0140-
6736(10)60549-1.
[2] Casey RM, Dumolard L, Danovaro-Holliday MC, Gacic-Dobo M, Diallo MS, Hampton LM, et al. Global
Routine Vaccination Coverage, 2015. MMWR Morb Mortal Wkly Rep 2016;65:1270–3.
[3] Simons E, Ferrari M, Fricks J, Wannemuehler K, Anand A, Burton A, et al. Assessment of the 2010 global
measles mortality reduction goal: results from a model of surveillance data. Lancet (London, England)
2012;379:2173–8. doi:10.1016/S0140-6736(12)60522-4.
[4] World Health Organization, UNICEF. WHO-UNICEF estimates of Pol3 coverage 2016.
http://apps.who.int/immunization_monitoring/globalsummary/timeseries/tswucoveragepol3.html.
[5] Immunization Technical Support Unit. Immunization Dashboard, December 2014 2014.
http://www.itsu.org.in/download.php?f=ITSU_Dashboard_Dec_2014.pdf.
[6] World Health Organization. Global Health Observatory Data Repository 2011.
http://apps.who.int/gho/data/?theme=main (accessed May 23, 2016).
[7] GOI and UNICEF (Government of India and United Nations Children’s Fund). 2009 Coverage Evaluation
Survey—All India Report 2010. http://files.givewell.org/files/DWDA 2009/GAIN/UNICEF India Coverage
Evaluation%0A Survey (2009).pdf%0A.
[8] Levin A, Kaddar M. Role of the private sector in the provision of immunization services in low- and
middle-income countries. Health Policy Plan 2011;26 Suppl 1:i4-12. doi:10.1093/heapol/czr037.
[9] Sridhar S, Maleq N, Guillermet E, Colombini A, Gessner BD. A systematic literature review of missed
opportunities for immunization in low- and middle-income countries. Vaccine 2014;32:6870–9.
doi:10.1016/j.vaccine.2014.10.063.
[10] Thacker N, Choudhury P, Gargano LM, Weiss PS, Pazol K, Bahl S, et al. Comparison of attitudes about
polio, polio immunization, and barriers to polio eradication between primary health center physicians
and private pediatricians in India. Int J Infect Dis 2012;16:e417-23. doi:10.1016/j.ijid.2012.02.002.
[11] Gargano LM, Thacker N, Choudhury P, Weiss PS, Pazol K, Bahl S, et al. Predictors of administration and
attitudes about pneumococcal, Haemophilus influenzae type b and rotavirus vaccines among
pediatricians in India: a national survey. Vaccine 2012;30:3541–5. doi:10.1016/j.vaccine.2012.03.064.
[12] Gargano LM, Thacker N, Choudhury P, Weiss PS, Pazol K, Bahl S, et al. Attitudes of pediatricians and
primary health center physicians in India concerning routine immunization, barriers to vaccination, and
missed opportunities to vaccinate. Pediatr Infect Dis J 2012;31:e37-42.
doi:10.1097/INF.0b013e3182433bb3.
[13] Sadler GR, Lee H-C, Lim RS-H, Fullerton J. Recruitment of hard-to-reach population subgroups via
adaptations of the snowball sampling strategy. Nurs Heal Sci 2010;12:369–74.
[14] Harris PA, Taylor R, Thielke R, Payne J, Gonzalez N, Conde JG. Research electronic data capture (REDCap)-
-a metadata-driven methodology and workflow process for providing translational research informatics
support. J Biomed Inform 2009;42:377–81. doi:10.1016/j.jbi.2008.08.010.
[15] R Core Team. R: A language and environment for statistical computing. R Foundation for Statistical
Computing, Vienna, Austria, 2012 2014.
[16] Benjamini Y, Hochberg Y. Controlling the False Discovery Rate : A Practical and Powerful Approach to
Multiple Testing Author ( s ): Yoav Benjamini and Yosef Hochberg Source : Journal of the Royal Statistical
Society . Series B ( Methodological ), Vol . 57 , No . 1 Published by : J R Stat Soc Ser B 1995;57:289–300.
[17] Vashishtha VM, Choudhury P, Kalra A, Bose A, Thacker N, Yewale VN, et al. Indian Academy of Pediatrics
(IAP) recommended immunization schedule for children aged 0 through 18 years -- India, 2014 and
updates on immunization. Indian Pediatr 2014;51:785–800. doi:10.1007/s13312-014-0504-y.
[18] Schaffer SJ, Szilagyi PG, Shone LP, Ambrose SJ, Dunn MK, Barth RD, et al. Physician perspectives regarding
pneumococcal conjugate vaccine. Pediatrics 2002;110:e68.
[19] Meyerhoff AS, Jacobs RJ. Do too many shots due lead to missed vaccination opportunities? Does it
matter? Prev Med (Baltim) 2005;41:540–4. doi:10.1016/j.ypmed.2004.12.001.
[20] Hanna JN, Bullen RC, Andrews DE. The acceptance of three simultaneous vaccine injections
recommended at 12 months of age. Commun Dis Intell Q Rep 2004;28:493–6.
[21] Kolasa MS, Petersen TJ, Brink EW, Bulim ID, Stevenson JM, Rodewald LE. Impact of multiple injections on
immunization rates among vulnerable children. Am J Prev Med 2001;21:261–6.
[22] Soeung SC, Grundy J, Morn C, Samnang C. Evaluation of immunization knowledge, practices, and service-
delivery in the private sector in Cambodia. J Health Popul Nutr 2008;26:95–104.
[23] United States Community Preventive Services Task Force. Increasing Appropriate Vaccination: Provider
Assessment and Feedback. Community Guid 2015.
https://www.thecommunityguide.org/findings/vaccination-programs-provider-assessment-and-feedback
(accessed January 3, 2017).
[24] Strategic Advisory Group of Experts on Immunization. Meeting of the Strategic Advisory Group of Experts
on immunization, April 2016– conclusions and recommendations. Wkly Epidemiol Rec 2016;21:265–84.
[25] World Health Organization. Missed Opportunities for Vaccination (MOV) Strategy 2017.
http://www.who.int/immunization/programmes_systems/policies_strategies/MOV/en/ (accessed
February 17, 2017).